Hebeloma erebium (Photo: H. J. Beker)

Taxonomy

Basionym:
Naucoria erebia Huijsman, Kew Bulletin 31 (3): 585 (1977)

Types: NETHERLANDS: Island of Voorne, Rockanj "Quackjeswater", Zuid-Holland (approx. 51.87°N, 4.0651°E, alt. approx. 0 m a.s.l.) on boggy, sandy soil in coastal dune under Betula sp. and Salix sp., 12 Jul. 1972, H.S.C. Huijsman (H72-80) (Holotype. herbarium acc. no. L0053546, HJB1000246).

Heterotypic synonyms:

• Hebeloma clavulipes var. hygrophanicum Bon, Documents mycologiques 23 (92): 42 (1994)

Homotypic synonyms:

• Alnicola erebia (Huijsman) Romagn., Bulletin trimestriel de la Fédération Mycologique Dauphiné-Savoie 74: 19 (1979)

• arrow_drop_downarrow_drop_upEtymology
  From erebius– (Greek) dark, from the nether-world; the name has been chosen because this species resembles very much a ringless Agrocybe erebia.

• arrow_drop_downarrow_drop_upOriginal diagnosis
  Habitu Agrocybe erebiae exannulatae. Pileo 30–70 mm, subregulari, mox expanso, plano-convexo vel obtusissime conico, hygrophano, sordide brunneo, exstriato, velo nullo. Lamellis subconfertis, 4–5 mm latis, adnatis, interdum leviter subdecurrentibus, pallide rufo-brunneis, ad aciem fimbriatam albidis. Stipite 50–80 x 4–8 mm, aequali, cavo, pileo multo palli-diore, apice leviter furfuraceo, ceterum glabro. Carne subconcolori; odore saporeque subnullis. Sporis 9–11 x 5–6.3 µm, amygdaliformibus, punctatis, crasso-tunicatis, ocraceis. Basidiis 4(-2)-sterigmatibus. Cheilocystidiis vulgo cylindricis vel subcylindricis, interdum subclavatis sed numquam capitatis, obtusis, 4–8 µm latis. Pleurocystidiis nullis. Pelle pilei cellulis polygonalibus multistratis instructa, hyphis sparsis laxe textis obducta. Fibulis numerosis. (Fig. I.) [Fig. 49.4 (colour)] Sub Betula solitaria Salicibus circumdata, loco humido, prope lacum parvum ‘Quackjeswater’, insulae Voorne, Nederland, 12 Jul. 1972, Huijsman (holotypus, L).

• arrow_drop_downarrow_drop_upEnglish translation
  Habit of a ringless Agrocybe erebia. Pileus 30–70 mm, subregular, soon expanded, plano-convex or very obtusely conical, hygrophanous, sordid brown, non-striate, veil absent. Lamellae crowded, 4–5 mm broad, adnate, occasionally slightly decurrent, pale reddish-brown, with white fimbriate edge. Stipe 50–80 × 4–8 mm, equal, hollow, much paler than the pileus, slightly furfuraceous at the apex, smooth elsewhere. Context concolorous; odour and taste almost absent. Spores 9–11 × 5–6.3 μm, amygdaloid, dotted, thick-walled, ochraceous. Basidia with four (to two) sterigmata. Cheilocystidia generally subcylindrical, occasionally subclavate but nowhere capitate, obtuse, 4–8 μm wide. Pleurocystidia none. Pileipellis consisting of multilayered polygonal cells surmounted by sparse loosely arranged hyphae. Clamps numerous. Under a solitary birch surrounded by willows, in a wet place, near “Quackjeswater”, a little lake on the isle of Voorne, the Netherlands, 12 Jul. 1972, Huijsman (holotype, L).

Description

Description of Hebeloma erebium based on 15 collections

• arrow_drop_downarrow_drop_upMacroscopic description
  Pileus: (22) 25–48 (70) mm diameter; shape often convex, occasionally umbonate or broadly umbonate, rarely weakly umbonate or strongly umbonate; characters occasionally hygrophanous, rarely remains of universal veil or rugulose; margin characters often smooth, rarely involute; viscosity tacky when moist; colour variation often two color, occasionally unicolour; colour at centre occasionally ochraceous or yellowish brown, rarely cinnamon or cream.

  Lamellae: attachment often emarginate, occasionally adnate, rarely decurrent tooth; maximum depth 5–6 mm; number of complete lamellae 50–74; presence of tears often absent, occasionally visible with x10 lens or visible with naked eye; white fimbriate edge often present, occasionally weak.

  Cortina presence: no.

  Stipe: (25) 30–63 (85) x 3–6 (8) {median} x (3) 4–9 (13) {basal} mm; stipe Q 3.8–16.7; base shape often clavate, occasionally bulbous, cylindrical or subbulbous; floccosity often velute, occasionally pruinose, rarely floccose, floccose at apex, pruinose at apex or tomentose; rooting no; thick rhizoids at base usually absent, occasionally present;

  Context: Texture firm; stipe interior hollow, occasionally superior wick; stipe flesh discolouring often yes, occasionally weak or no; slenderness measure 5.0–19.9; smell occasionally raphanoid or strongly raphanoid, rarely odourless or weakly raphanoid; taste often none or weakly raphanoid where recorded.

  Spore deposit colour: brownish olive.

  Exsiccata characters: often fragile, occasionally lamellae blackening or pale.

• arrow_drop_downarrow_drop_upMicroscopic description
  Spores: shape amygdaloid, usually limoniform; colour in microscope often brown, occasionally yellow or yellow brown; guttules variable. papilla often yes, occasionally very strongly; Spore Code: O2 O3; P1 (P2); (D2) D3.

  Basidia: 23–39 (42) x 7–11 μm; ave. Q 2.5–4.6; spore arrangement Not recorded;

  Cheilocystidia: main shape ventricose, usually clavate-lageniform or clavate-ventricose, lageniform or gently clavate, occasionally clavate, rarely cylindrical or utriform; special features observed often geniculate, occasionally septa, bifurcate or median thickening, rarely apical thickening, branching, clamped septa, many collapsed in exsiccata, yellow contents or spathulate; cheilocystidia ratios: A/M = 1.25–1.68; A/B = 0.78–1.18; B/M = 1.35–1.74.

  Pleurocystidia: usually none seen, rarely only close to lamella edge.

  Ixocutis: epicutis thickness (measured from exsiccata) up to 80 μm; ixocutis hyphae width up to 5 μm; ixocutis hyphae encrustation yes; shape of trama elements beneath subcutis thickly sausage-shaped, often ellipsoid up to 27 μm wide.

  Caulocystidia: Similar to cheilocystidia but larger, up to 150 μm.

• arrow_drop_downarrow_drop_upSpore measurements

• arrow_drop_downarrow_drop_upCheilocystidia measurements

• arrow_drop_downarrow_drop_upHabitat and distribution
  Hebeloma erebium's preferred habitat appears to be mixed woodland. Where only one possible associate was recorded, the most commonly recorded associate was Tilia (40.0%) but Fagus (40.0%) and Salix (20.0%) were also recorded. In these cases the most commonly recorded families were Malvaceae (40.0%), Fagaceae (40.0%) and Salicaceae (20.0%). We have additional records where Quercus (40.0%), Carpinus (33.3%), Betula (20.0%), Alnus (13.3%), Populus (13.3%), Corylus (6.7%), Picea (6.7%) and Pinus (6.7%) were recorded as possible associates, but in these cases a number of possible associates were mentioned. Overall the most commonly recorded families are Betulaceae (60.0%), Fagaceae (53.3%), Salicaceae (33.3%), Malvaceae (20.0%) and Pinaceae (13.3%) The growth habit of our collections was often scattered, occasionally solitary and rarely gregarious.

  According to our current collections, the species is found only in Europe. On the continent, collections have been found only in the temperate broadleaf & mixed forests WWF biome The World Wildlife Fund (WWF) have divided the world into 867 terrestrial ecoregions. The ecoregion here is estimated by mapping from the GPS coordinates of the collection using data made available by Dinerstein et al (2017). Use this webtool to explore the ecoregions visually or see a full list of current ecoregions on Wikipedia. (European Atlantic mixed forests (26.7%), Central European mixed forests (26.7%), Pannonian mixed forests (13.3%) and Western European broadleaf forests (13.3%) ecoregions). From collector information, it appears collections have been found only in the 1.4 Forest – Temperate IUCN habitat We map from the collector's description of the habitat to the International Union for Conservation of Nature (IUCN)'s definition using a standardised set of rules. Please see this page for a full list of IUCN habitats.. Within Europe we have records from the Centre (Poland, Austria, Germany, Belgium and Netherlands), Eastern Europe (Estonia), the Southwest (France) and the North (Denmark). Specimens have been collected from 48.1°N to 59.0°N.

• arrow_drop_downarrow_drop_upMolecular results
  This species can be recognized by all tested loci apart from ITS. With ITS, H. erebium cannot be differentiated from H. celatum and H. quercetorum. The identity of this taxon with H. erebium is supported not only by ITS but also by mitochondrial sequences (V6 and V9) from the type of H. erebium. Mitochondrial loci also support the synonymization of the invalidly published H. clavulipes var. hygrophanicum with H. erebium. There are two published ITS sequences from Asia (Iran, Mongolia) that are likely to belong to a member of the quercetorum-complex (FR852300; FJ803967 with Populus davidiana).

• arrow_drop_downarrow_drop_upCommentary
  Hebeloma erebium has a mixture of differently shaped cheilocystidia and, in our experience, the ratios of the different cheilocystidia vary. This taxon has ventricose or lageniform cheilocystidia that are mixed with more gently clavate cheilocystidia, wider at the apex and tapering below. There are also usually intermediates which are clavate-lageniform, i.e. swollen both at the apex and in the basal part. The large number of ventricose lageniform) cheilocystidia, the distinctly ornamented, rather strongly dextrinoid spores plus the absence of any obvious cortina or veil, places this taxon in either H. sects. Sinapizantia or Velutipes. (It should be noted that there is a possible confusion between this species and species within H. sect. Denudata subsect. Echinospora, but species within this latter section do not have ventricose cheilocystidia where the upper part is fairly cylindrical.) Within H. sect. Sinapizantia, and with the large number of ventricose cheilocystidia, it can be confused with H. sinapizans. However, it is easily separated from H. sinapizans: macroscopically, by the occasional presence of tears, the lower number of lamellae and the less robust appearance; microscopically, by the presence of gently clavate and clavate-lageniform cheilocystidia. Both these taxa have a cheilocystidium ratio B/M that is at least 1.35. With H. sinapizans this ratio usually exceeds 1.5, but with H. erebium this ratio depends on the balance between the different types of cheilocystidia present and measured. Within H. sect. Velutipes, Hebeloma erebium is within the quercetorum-complex and hence it is very closely related, both phylogenetically and morphologically to H. quercetorum and H. celatum. With regard to H. quercetorum there is a clear biogeographical separation. We have no records of H. erebium further south than the latitude of 48 deg N, while we have no records of H. quercetorum further north than latitude 44.5 deg N. Of course it may be possible that H. erebium may occur further south, but if so we would expect it to occur in higher altitude areas. Also of note is that H. quercetorum appears to be restricted to Quercus as a host, whereas H. erebium has been recorded with many different hosts; more collections will help determine whether this taxon really does have ectomycorrhizal associations with such a wide variety of hosts. Further, H. quercetorum has a far thicker epicutis than H. erebium, in the range 160–200 μm while H. erebium has its epicutis thickness in the range 60–80 μm. The cheilocystidia of H. quercetorum are more regularly lageniform to ventricose to cylindrical while H. erebium has more cheilocystidia that are clearly gently clavate or clavate-lageniform. With respect to H. celatum, which also appears to favour Southern Europe, but does also occur in Northern Europe, the latter species tends to have a more robust appearance and this is reflected in the stipe width, which, for mature basidiomes, is normally more than 8 mm wide at its median point and more than 13 mm wide at the base. This contrasts with the stipe width of H. erebium which is always less than 8 mm at its median point and never greater than 13 mm at its base. Hebeloma erebium is macroscopically similar to H. aestivale and both taxa favour very similar habitats. A macroscopic difference which can be useful in the field is the number of full length lamellae (L): for H. aestivale this is 35–59 with average 50 while for H. erebium L = 50–75 with average over 60. Microscopically these two taxa are very easy to separate both on the cheilocystidia, which are quite different, and the spores where H. aestivale has a strongly and constantly loosening perispore. Moreau (2005) in his nomenclature revision of Alnicola pointed out that Alnicola erebia had been described by Huijsman (1977) as having clamp connections and may indeed be a Hebeloma. It was also P.-A. Moreau who originally suggested to us that we should examine the type of this taxon.

Geographic distribution

Phenology

• arrow_drop_downarrow_drop_upAdditional cited collections

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